Industrial Melanism in British Peppered Moths Has a Singular and Recent Mutational Origin

Abstract

The rapid spread of a novel black form (known as carbonaria) of the peppered moth Biston betularia in 19th-century Britain is a textbook example of how an altered environment may produce morphological adaptation through genetic change. However, the underlying genetic basis of the difference between the wild-type (light-colored) and carbonaria forms has remained unknown. We have genetically mapped the carbonaria morph to a 200-kilobase region orthologous to a segment of silkworm chromosome 17 and show that there is only one core sequence variant associated with the carbonaria morph, carrying a signature of recent strong selection. The carbonaria region coincides with major wing-patterning loci in other lepidopteran systems, suggesting the existence of basal color-patterning regulators in this region.

Mapping and recombination analysis of two moth colour mutations, Black moth and Wild wing spot, in the silkworm Bombyx mori

“…Therefore, recombination between both genes occurred in none of the individuals. Moreover, we found that the candidate regions of both genes shared correspondence with a region associated with wing-and body-colour variations in different lepidopteran species, that is, B. betularia, Heliconius cydno, Heliconius erato, Heliconius melpomene and Heliconius numata (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011). These results strongly suggest that the same genes and/or regulatory elements responsible for wing and body colour in Bombyx, Bm and Ws, may underlie these variants in different Lepidoptera.…”

“…The genetic and genomic analysis demonstrated the following: (i) the candidate regions of the Bm and Ws genes are located in~2-Mb-long and 100-kb-long regions on the same scaffold Bm_scaf33 of chromosome 17; (ii) chromosome 17 of Bm mutation harbours inversion within a compartment corresponding to Bm_scaf33; and (iii) the Bm and Ws regions share synteny with a region associated with wing-and body-colour variations in different lepidopteran species (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011). Based on our results, we hypothesise that this common region may control wingand body-colour variations in lepidopteran insects.…”

“…Comparative genomic analysis of the Bm and Ws regions, and other lepidopteran genomes Based on the comparative genomic analysis, we found that the Bm and Ws regions shared synteny with a region associated with wing-and body-colour variations in different lepidopteran species of B. betularia and Heliconius butterflies (Joron et al, 2006;Kronfost et al, 2006;Papa et al, 2008;Ferguson et al, 2010;van't Hof et al, 2011 (Figure 4). Both of these causal genes determine wing colour variations in H. melpomene (Ferguson et al, 2010 Table 1 for details of the BAC probe information.…”

The peppered moth and industrial melanism: evolution of a natural selection case study

“…Informed by results from Drosophila (Wittkopp et al, 2003) and Papilio xuthus (Koch et al, 2000), it was initially thought likely that the developmental switch for melanism would be found within the canonical melanisation pathway (True, 2003). A survey of all the candidate genes revealed that this is not the case ( Van't Hof and Saccheri, 2010), paving the way for a genome-wide segregation analysis of amplified fragment length polymorphisms, which localised the carbonaria locus to a chromosomal region with no known function in melanisation ( Van't Hof et al, 2011). Curiously, and quite unexpectedly, the carbonaria region is orthologous to a major wing patterning locus controlling mimicry forms in Heliconius butterflies (Papa et al, 2008;Joron et al, 2011).…”

“…Patterns of linkage disequilibrium around the melanism locus indicate that, throughout the United Kingdom, the melanic morph carbonaria is descended from a single mutational event in the recent past ( Van't Hof et al, 2011), thus settling the question whether industrial melanism arose several times in Britain and showing that the initial extension of range was a result of migration. Ongoing work aims to document the genetic consequences of the rise and fall of carbonaria, principally by analysing changes in linkage disequilibrium and nucleotide diversity along the north Wales, north-west England cline through time, using archival material.…”